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VOLUME 2 , ISSUE 3 ( July-September, 2023 ) > List of Articles


Extrauterine Growth Restriction: Need for an Accurate Definition

Nalinikanta Panigrahi, Aaron Germain, Ilhama Namazova, Ola Didrik Saugstad

Keywords : Body fat mass, Cohort of Indonesian PreTerm infants for long-term Outcomes study, Corrected gestational age, Delta-Z, Demographic factors, Extra-uterine growth restriction, Failure to thrive, Fenton growth chart, Genetic make-up, growth charts, Infant growth, Intra-uterine growth restriction, Intergrowth 21st charts, Infant feeding, Linear growth velocity, Maternal metabolism, Maternal and paternal anthropometrics, Medications, Newborn, Neonate, Neurodevelopmental outcomes, Neonatal morbidities, Placental health, Postnatal growth restriction, Postnatal malnutrition, Pre-conceptional nutritional status, Postnatal morbidities, Postnatal growth, Small for gestation, Term corrected age, Total caloric intake, Total metabolic activity, Weight gain velocity, Z-scores

Citation Information : Panigrahi N, Germain A, Namazova I, Saugstad OD. Extrauterine Growth Restriction: Need for an Accurate Definition. 2023; 2 (3):198-202.

DOI: 10.5005/jp-journals-11002-0072

License: CC BY-NC 4.0

Published Online: 26-09-2023

Copyright Statement:  Copyright © 2023; The Author(s).


Neonates show considerable variation in growth that can be recognized through serial measurements of basic variables such as weight, length, and head circumference. If possible, measurement of subcutaneous and total body fat mass can also be useful. These biometric measurements at birth may be influenced by demographics, maternal and paternal anthropometrics, maternal metabolism, preconceptional nutritional status, and placental health. Subsequent growth may depend on optimal feeding, total caloric intake, total metabolic activity, genetic makeup, postnatal morbidities, medications, and environmental conditions. For premature infants, these factors become even more important; poor in utero growth can be an important reason for spontaneous or induced preterm delivery. Later, many infants who have had intrauterine growth restriction (IUGR) and are born small for gestational age (SGA) continue to show suboptimal growth below the 10th percentile, a condition that has been defined as extrauterine growth restriction (EUGR) or postnatal growth restriction (PNGR). More importantly, a subset of these growth-restricted infants may also be at high risk of abnormal neurodevelopmental outcomes. There is a need for well-defined criteria to recognize EUGR/PNGR, so that correctional steps can be instituted in a timely fashion.

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  1. Euser AM, de Wit CC, Finken MJ, et al. Growth of preterm born children. Horm Res 2008;70(6):319–328. DOI: 10.1159/000161862.
  2. Bagga N, Reddy KK, Mohamed A, et al. Quality improvement initiative to decrease extrauterine growth restriction in preterm neonates. Nutr Clin Pract 2021;36(6):1296–1303. DOI: 10.1002/ncp.10735.
  3. Fenton TR, Chan HT, Madhu A, et al. Preterm infant growth velocity calculations: A systematic review. Pediatrics 2017;139(3):e20162045. DOI: 10.1542/peds.2016-2045.
  4. Hack M, Merkatz IR, Gordon D, Jet al. The prognostic significance of postnatal growth in very low birth weight infants. Am J Obstet Gynecol 1982;143(6):693–699. DOI: 10.1016/0002-9378(82)90117-x.
  5. Goldberg DL, Becker PJ, Brigham K, et al. Identifying malnutrition in preterm and neonatal populations: Recommended indicators. J Acad Nutr Diet 2018;118(9):1571–1582. DOI: 10.1016/j.jand.2017.10.006.
  6. Shah PS, Wong KY, Merko S, et al. Postnatal growth failure in preterm infants: Ascertainment and relation to long-term outcome. J Perinat Med 2006;34(6):484–489. DOI: 10.1515/JPM.2006.094.
  7. Zozaya C, Diaz C, de Pipaon MS. How should we define postnatal growth restriction in preterm infants? Neonatology 2018;114(2): 177–180. DOI: 10.1159/000489388.
  8. Tudehope DI, Burns Y, O'Callaghan M, et al. The relationship between intrauterine and postnatal growth on the subsequent psychomotor development of very low birthweight (VLBW) infants. Aust Paediatr J 1983;19(1):3–8. DOI: 10.1111/j.1440-1754.1983.tb02041.x.
  9. Fenton TR, Kim JH. A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr 2013;13:59. DOI: 10.1186/1471-2431-13-59.
  10. Cole TJ, Williams AF, Wright CM, et al. Revised birth centiles for weight, length and head circumference in the UK-WHO growth charts. Ann Hum Biol 2011;38(1):7–11. DOI: 10.3109/03014460.2011.544139.
  11. Bertino E, Coscia A, Mombro M, et al. Postnatal weight increase and growth velocity of very low birthweight infants. Arch Dis Child Fetal Neonatal Ed 2006;91(5):F349–F356. DOI: 10.1136/adc.2005.090993.
  12. Rochow N, Raja P, Liu K, et al. Physiological adjustment to postnatal growth trajectories in healthy preterm infants. Pediatr Res 2016;79(6):870–879. DOI: 10.1038/pr.2016.15.
  13. Cole TJ, Statnikov Y, Santhakumaran S, et al. Birth weight and longitudinal growth in infants born below 32 weeks’ gestation: A UK population study. Arch Dis Child Fetal Neonatal Ed 2014;99(1): F34–F40. DOI: 10.1136/archdischild-2012-303536.
  14. Franz AR, Pohlandt F, Bode H, et al. Intrauterine, early neonatal, and postdischarge growth and neurodevelopmental outcome at 5.4 years in extremely preterm infants after intensive neonatal nutritional support. Pediatrics 2009;123(1):e101–e109. DOI: 10.1542/peds.2008-1352.
  15. Ehrenkranz RA, Younes N, Lemons JA, et al. Longitudinal growth of hospitalized very low birth weight infants. Pediatrics 1999;104 (2 Pt 1):280–289. DOI: 10.1542/peds.104.2.280.
  16. Belfort MB, Gillman MW, Buka SL, et al. Preterm infant linear growth and adiposity gain: Trade-offs for later weight status and intelligence quotient. J Pediatr 2013;163(6):1564.e2–1569.e2. DOI: 10.1016/j.jpeds.2013.06.032.
  17. Dusick AM, Poindexter BB, Ehrenkranz RA, et al. Growth failure in the preterm infant: Can we catch up? Semin Perinatol 2003;27(4):302–310. DOI: 10.1016/s0146-0005(03)00044-2.
  18. Raghuram K, Yang J, Church PT, et al. Head growth trajectory and neurodevelopmental outcomes in preterm neonates. Pediatrics 2017;140(1):e20170216. DOI: 10.1542/peds.2017-0216.
  19. Georgieff MK, Hoffman JS, Pereira GR, et al. Effect of neonatal caloric deprivation on head growth and 1-year developmental status in preterm infants. J Pediatr 1985;107(4):581–587. DOI: 10.1016/s0022-3476(85)80028-7.
  20. Sammallahti S, Pyhala R, Lahti M, et al. Infant growth after preterm birth and neurocognitive abilities in young adulthood. J Pediatr 2014;165(6):1109.e3–1115.e3. DOI: 10.1016/j.jpeds.2014.08.028.
  21. Nitasha Bagga, Nalinikant Panigrahay, Akhil Maheshwari. Extra-uterine growth restriction in preterm infants. Newborn 2022;1(1): 67–73. DOI: 10.5005/jp-journals-11002-0019.
  22. Fenton TR, Cormack B, Goldberg D, et al. “Extrauterine growth restriction” and “postnatal growth failure” are misnomers for preterm infants. J Perinatol 2020;40(5):704–714. DOI: 10.1038/s41372-020-0658-5.
  23. Peila C, Spada E, Giuliani F, et al. Extrauterine growth restriction: Definitions and predictability of outcomes in a cohort of very low birth weight infants or preterm neonates. Nutrients 2020;12(5):1224. DOI: 10.3390/nu12051224.
  24. Rohsiswatmo R, Kaban RK, Sjahrulla MAR, et al. Defining postnatal growth failure among preterm infants in Indonesia. Front Nutr 2023;10:1101048. DOI: 10.3389/fnut.2023.1101048.
  25. Shlomai NO, Reichman B, Lerner–Geva L, et al. Population-based study shows improved postnatal growth in preterm very-low-birthweight infants between 1995 and 2010. Acta Paediatr 2014;103(5):498–503. DOI: 10.1111/apa.12569.
  26. Clark RH, Thomas P, Peabody J. Extrauterine growth restriction remains a serious problem in prematurely born neonates. Pediatrics 2003;111(5 Pt 1):986–990. DOI: 10.1542/peds.111.5.986.
  27. Cooke RJ, Ainsworth SB, Fenton AC. Postnatal growth retardation: A universal problem in preterm infants. Arch Dis Child Fetal Neonatal Ed 2004;89(5):F428–F430. DOI: 10.1136/adc.2001.004044.
  28. Embleton NE, Pang N, Cooke RJ. Postnatal malnutrition and growth retardation: An inevitable consequence of current recommendations in preterm infants? Pediatrics 2001;107(2):270–273. DOI: 10.1542/peds.107.2.270.
  29. Roggero P, Gianni ML, Amato O, et al. Postnatal growth failure in preterm infants: recovery of growth and body composition after term. Early Hum Dev 2008;84(8):555–559. DOI: 10.1016/j.earlhumdev.2008.01.012.
  30. Fenton TR, Nasser R, Eliasziw M, et al. Validating the weight gain of preterm infants between the reference growth curve of the fetus and the term infant. BMC Pediatr 2013;13:92. DOI: 10.1186/1471-2431-13-92.
  31. Niklasson A, Albertsson–Wikland K. Continuous growth reference from 24th week of gestation to 24 months by gender. BMC Pediatr 2008;8:8. DOI: 10.1186/1471-2431-8-8.
  32. Berry MA, Abrahamowicz M, Usher RH. Factors associated with growth of extremely premature infants during initial hospitalization. Pediatrics 1997;100(4):640–646. PMID: 9310518.
  33. Carlson SJ, Ziegler EE. Nutrient intakes and growth of very low birth weight infants. J Perinatol 1998;18(4):252–258. PMID: 9730193.
  34. Martin CR, Brown YF, Ehrenkranz RA, et al. Nutritional practices and growth velocity in the first month of life in extremely premature infants. Pediatrics 2009;124(2):649–657. DOI: 10.1542/peds.2008-3258.
  35. Villar J, Giuliani F, Barros F, et al. Monitoring the postnatal growth of preterm infants: A paradigm change. Pediatrics 2018;141(2):e20172467. DOI: 10.1542/peds.2017-2467.
  36. Horbar JD, Ehrenkranz RA, Badger GJ, et al. Weight growth velocity and postnatal growth failure in infants 501 to 1500 grams: 2000–2013. Pediatrics 2015;136(1):e84–e92. DOI: 10.1542/peds.2015-0129.
  37. Radmacher PG, Looney SW, Rafail ST, et al. Prediction of extrauterine growth retardation (EUGR) in VVLBW infants. J Perinatol 2003;23(5):392–395. DOI: 10.1038/
  38. Papageorghiou AT, Kennedy SH, Salomon LJ, et al. The INTERGROWTH-21st fetal growth standards: Toward the global integration of pregnancy and pediatric care. Am J Obstet Gynecol 2018;218(2S):S630–S640. DOI: 10.1016/j.ajog.2018.01.011.
  39. Salas AA, Bhatia A, Carlo WA. Postnatal growth of preterm infants 24 to 26 weeks of gestation and cognitive outcomes at 2 years of age. Pediatr Res 2021;89(7):1804–1809. DOI: 10.1038/s41390-020-01158-y.
  40. Tuzun F, Yucesoy E, Baysal B, et al. Comparison of INTERGROWTH-21 and Fenton growth standards to assess size at birth and extrauterine growth in very preterm infants. J Matern Fetal Neonatal Med 2018;31(17):2252–2257. DOI: 10.1080/14767058.2017.1339270.
  41. Kim YJ, Shin SH, Cho H, et al. Extrauterine growth restriction in extremely preterm infants based on the Intergrowth-21st Project Preterm Postnatal Follow-up Study growth charts and the Fenton growth charts. Eur J Pediatr 2021;180(3):817–824. DOI: 10.1007/s00431-020-03796-0.
  42. Reddy KV, Sharma D, Vardhelli V, et al. Comparison of Fenton 2013 growth curves and Intergrowth-21 growth standards to assess the incidence of intrauterine growth restriction and extrauterine growth restriction in preterm neonates ≤32 weeks. J Matern Fetal Neonatal Med 2021;34(16):2634–2641. DOI: 10.1080/14767058.2019.1670795.
  43. Liu S, Metcalfe A, Leon JA, et al. Evaluation of the INTERGROWTH-21st project newborn standard for use in Canada. PLoS One 2017;12(3):e0172910. DOI: 10.1371/journal.pone.0172910.
  44. Samarani M, Restom G, Mardini J, et al. Comparative study between Fenton and intergrowth 21 charts in a sample of Lebanese premature babies. BMC Pediatr 2020;20(1):74. DOI: 10.1186/s12887-020-1968-7.
  45. Yitayew M, Chahin N, Rustom S, et al. Fenton vs. Intergrowth-21st: Postnatal growth assessment and prediction of neurodevelopment in preterm infants. Nutrients 2021;13(8):2841. DOI: 10.3390/nu13082841.
  46. Johnson MJ, Wootton SA, Leaf AA, et al. Preterm birth and body composition at term equivalent age: A systematic review and meta-analysis. Pediatrics 2012;130(3):e640–e649. DOI: 10.1542/peds.2011-3379.
  47. Gianni ML, Roggero P, Piemontese P, et al. Boys who are born preterm show a relative lack of fat-free mass at 5 years of age compared to their peers. Acta Paediatr 2015;104(3):e119–e123. DOI: 10.1111/apa.12856.
  48. Heimler R, Doumas BT, Jendrzejczak BM, et al. Relationship between nutrition, weight change, and fluid compartments in preterm infants during the first week of life. J Pediatr 1993;122(1):110–114. DOI: 10.1016/s0022-3476(05)83502-4.
  49. Lorenz JM, Kleinman LI, Ahmed G, et al. Phases of fluid and electrolyte homeostasis in the extremely low birth weight infant. Pediatrics 1995;96(3 Pt 1):484–489.
  50. de Onis M. The use of anthropometry in the prevention of childhood overweight and obesity. Int J Obes Relat Metab Disord 2004;28 (Suppl. 3):S81–S85. DOI: 10.1038/sj.ijo.0802810.
  51. Lorch SA. The clinical and policy implications of new measures of premature infant growth. Pediatrics 2015;135(3):e703–e704. DOI: 10.1542/peds.2014-3774.
  52. Al-Theyab NA, Donovan TJ, Eiby YA, et al. Fat trajectory after birth in very preterm infants mimics healthy term infants. Pediatr Obes 2019;14(3):e12472. DOI: 10.1111/ijpo.12472.
  53. O'Connor DL, Gibbins S, Kiss A, et al. Effect of supplemental donor human milk compared with preterm formula on neurodevelopment of very low-birth-weight infants at 18 months: A randomized clinical trial. JAMA 2016;316(18):1897–1905. DOI: 10.1001/jama.2016.16144.
  54. Makrides M, Gibson RA, McPhee AJ, et al. Effect of DHA supplementation during pregnancy on maternal depression and neurodevelopment of young children: A randomized controlled trial. JAMA 2010;304(15):1675–1683. DOI: 10.1001/jama.2010.1507.
  55. Keim SA, Boone KM, Klebanoff MA, et al. Effect of docosahexaenoic acid supplementation vs placebo on developmental outcomes of toddlers born preterm: A randomized clinical trial. JAMA Pediatr 2018;172(12):1126–1134. DOI: 10.1001/jamapediatrics.2018.3082.
  56. Regev RH, Arnon S, Litmanovitz I, et al. Association between neonatal morbidities and head growth from birth until discharge in very-low-birthweight infants born preterm: A population-based study. Dev Med Child Neurol 2016;58(11):1159–1166. DOI: 10.1111/dmcn.13153.
  57. Belfort MB, Rifas–Shiman SL, Sullivan T, et al. Infant growth before and after term: Effects on neurodevelopment in preterm infants. Pediatrics 2011;128(4):e899–e906. DOI: 10.1542/peds.2011-0282.
  58. Ehrenkranz RA, Dusick AM, Vohr BR, et al. Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics 2006;117(4):1253–1261. DOI: 10.1542/peds.2005-1368.
  59. Ong KK, Kennedy K, Castaneda–Gutierrez E, et al. Postnatal growth in preterm infants and later health outcomes: A systematic review. Acta Paediatr 2015;104(10):974–986. DOI: 10.1111/apa.13128.
  60. Corpeleijn WE, Kouwenhoven SM, van Goudoever JB. Optimal growth of preterm infants. World Rev Nutr Diet 2013;106:149–155. DOI: 10.1159/000342584.
  61. Weisglas–Kuperus N, Hille ET, Duivenvoorden HJ, et al. Intelligence of very preterm or very low birthweight infants in young adulthood. Arch Dis Child Fetal Neonatal Ed 2009;94(3):F196–F200. DOI: 10.1136/adc.2007.135095.
  62. Pineda RG, Stransky KE, Rogers C, et al. The single-patient room in the NICU: Maternal and family effects. J Perinatol 2012;32(7):545–551. DOI: 10.1038/jp.2011.144.
  63. Benavente–Fernandez I, Synnes A, Grunau RE, et al. Association of socioeconomic status and brain injury with neurodevelopmental outcomes of very preterm children. JAMA Netw Open 2019;2(5): e192914. DOI: 10.1001/jamanetworkopen.2019.2914.
  64. Maheshwari A, Lui K, Motta M. Understanding the impact of maternal health on neonatal disease: A new horizon. Newborn 2023;1(4):iv–vi. DOI: 10.5005/newborn-1-4-iv.
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